Preattachment Embryos of Domestic Animals: Insights into Development and Paracrine Secretions.
Abstract: In mammalian species, endometrial receptivity is driven by maternal factors independently of embryo signals. When pregnancy initiates, paracrine secretions of the preattachment embryo are essential both for maternal recognition and endometrium preparation for implantation and for coordinating development of embryonic and extraembryonic tissues of the conceptus. This review mainly focuses on domestic large animal species. We first illustrate the major steps of preattachment embryo development, including elongation in bovine, ovine, porcine, and equine species. We next highlight conceptus secretions that are involved in the communication between extraembryonic and embryonic tissues, as well as between the conceptus and the endometrium. Finally, we introduce experimental data demonstrating the intimate connection between conceptus secretions and endometrial activity and how adverse events perturbing this interplay may affect the progression of implantation that will subsequently impact pregnancy outcome, postnatal health, and expression of production traits in livestock offspring.
Publication Date: 2016-12-05 PubMed ID: 27959670DOI: 10.1146/annurev-animal-022516-022900Google Scholar: Lookup
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Summary
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This research paper discusses the role of preattachment embryos in domestic animals, specifically looking at their development and the function of their paracrine secretions in maternal recognition and endometrium preparation. The paper pays special attention to large domestic animals such as cows, sheep, pigs, and horses, and explores how any disruption to the interaction between embryonic secretions and endometrial activity can have implications for not just pregnancy and postnatal health, but also on the animals’ performance as livestock.
Steps of Preattachment Embryo Development
The paper begins by outlining the key stages of development that a preattachment embryo goes through in large domestic animals:
- Elongation process in bovine, ovine, porcine, and equine species is detailed.
- The elongation process ensures the maximum surface area for nutrient exchange, which is essential for the growth and survival of the embryo.
- This embryo development stage is crucial as this is when the embryo shapes, prepares and aligns itself for successful attachment to the endometrium.
Conceptus Secretions and Communication
The research article then looks into the secretions produced by the conceptus—the embryo and its associated membranes—and how these secretions facilitate communication:
- The secretions play a vital role in transmitting signals to the endometrium and between different embryonic and extraembryonic tissues.
- These secretions act as messages that inform the mother’s body of the pregnancy, preparing the endometrium for implantation.
- Additionally, they help to coordinate the growth and development of various embryonic and extraembryonic tissues within the conceptus.
Conceptus Secretions and Endometrial Activity
Next, the research discusses experimental data that shows the close relationship between the conceptus’ secretions and the activity of the endometrium:
- A delicate communication network is established between the embryo and uterus through these secretions.
- This communication is integral for successful implantation, enabling the progression of pregnancy.
- Any disruption in this signaling can impact the embryo’s proper implantation into the endometrium and subsequently affect the pregnancy’s progression and outcome.
Impact of Adverse Events
In the final part of the article, the potential implications of any disruption to the interaction between the secretions and endometrial activity are addressed:
- Adverse events or disturbances affecting the secretion-endometrium interplay can potentially lead to unsuccessful implantation or other complications, affecting the pregnancy outcome.
- The disruptions could also have an influence on the offspring’s postnatal health and possibly its productivity as a livestock animal. The traits expressed in livestock offspring could be affected – altering meat quality, milk production, or overall robustness.
Cite This Article
APA
Sandra O, Charpigny G, Galio L, Hue I.
(2016).
Preattachment Embryos of Domestic Animals: Insights into Development and Paracrine Secretions.
Annu Rev Anim Biosci, 5, 205-228.
https://doi.org/10.1146/annurev-animal-022516-022900 Publication
Researcher Affiliations
- UMR BDR, INRA, ENVA, Université Paris Saclay, 78350, Jouy en Josas, France; email: olivier.sandra@inra.fr , gilles.charpigny@inra.fr , laurent.galio@inra.fr , isabelle.hue@inra.fr.
- UMR BDR, INRA, ENVA, Université Paris Saclay, 78350, Jouy en Josas, France; email: olivier.sandra@inra.fr , gilles.charpigny@inra.fr , laurent.galio@inra.fr , isabelle.hue@inra.fr.
- UMR BDR, INRA, ENVA, Université Paris Saclay, 78350, Jouy en Josas, France; email: olivier.sandra@inra.fr , gilles.charpigny@inra.fr , laurent.galio@inra.fr , isabelle.hue@inra.fr.
- UMR BDR, INRA, ENVA, Université Paris Saclay, 78350, Jouy en Josas, France; email: olivier.sandra@inra.fr , gilles.charpigny@inra.fr , laurent.galio@inra.fr , isabelle.hue@inra.fr.
MeSH Terms
- Animals
- Animals, Domestic
- Cattle
- Embryo Implantation
- Embryonic Development
- Endometrium / metabolism
- Female
- Horses
- Pregnancy
- Pregnancy Outcome
- Pregnancy, Animal / metabolism
- Sheep
- Swine
Citations
This article has been cited 14 times.- Kinoshita M, Kobayashi T, Planells B, Klisch D, Spindlow D, Masaki H, Bornelöv S, Stirparo GG, Matsunari H, Uchikura A, Lamas-Toranzo I, Nichols J, Nakauchi H, Nagashima H, Alberio R, Smith A. Pluripotent stem cells related to embryonic disc exhibit common self-renewal requirements in diverse livestock species. Development 2021 Dec 1;148(23).
- Kowalczyk A, Czerniawska-Piątkowska E, Wrzecińska M. The Importance of Interferon-Tau in the Diagnosis of Pregnancy. Biomed Res Int 2021;2021:9915814.
- Charpigny G, Marquant-Le Guienne B, Richard C, Adenot P, Dubois O, Gélin V, Peynot N, Daniel N, Brochard V, Nuttinck F. PGE2 Supplementation of Oocyte Culture Media Improves the Developmental and Cryotolerance Performance of Bovine Blastocysts Derived From a Serum-Free in vitro Production System, Mirroring the Inner Cell Mass Transcriptome. Front Cell Dev Biol 2021;9:672948.
- Carbonnel M, Cornet N, Revaux A, Favre-Inhofer A, Galio L, Raliou M, Couturier-Tarrade A, Giraud-Delville C, Charpigny G, Gelin V, Dubois O, Hersant B, Bosc R, Coscas R, Vialard F, Chavatte-Palmer P, Richard C, Sandra O, Ayoubi JM. Analysis of blood parameters and molecular endometrial markers during early reperfusion in two ovine models of uterus transplantation. PLoS One 2021;16(5):e0251474.
- Alberio R, Kobayashi T, Surani MA. Conserved features of non-primate bilaminar disc embryos and the germline. Stem Cell Reports 2021 May 11;16(5):1078-1092.
- Kumro FG, O'Neil EV, Ciernia LA, Moraes JGN, Spencer TE, Lucy MC. Scanning electron microscopy of the surface epithelium of the bovine endometrium. J Dairy Sci 2020 Dec;103(12):12083-12090.
- Recuero S, Sánchez JM, Mateo-Otero Y, Bagés-Arnal S, McDonald M, Behura SK, Spencer TE, Kenny DA, Yeste M, Lonergan P, Fernandez-Fuertes B. Mating to Intact, but Not Vasectomized, Males Elicits Changes in the Endometrial Transcriptome: Insights From the Bovine Model. Front Cell Dev Biol 2020;8:547.
- Eozenou C, Lesage-Padilla A, Mauffré V, Healey GD, Camous S, Bolifraud P, Giraud-Delville C, Vaiman D, Shimizu T, Miyamoto A, Sheldon IM, Constant F, Pannetier M, Sandra O. FOXL2 is a Progesterone Target Gene in the Endometrium of Ruminants. Int J Mol Sci 2020 Feb 21;21(4).
- Biase FH, Hue I, Dickinson SE, Jaffrezic F, Laloe D, Lewin HA, Sandra O. Fine-tuned adaptation of embryo-endometrium pairs at implantation revealed by transcriptome analyses in Bos taurus. PLoS Biol 2019 Apr;17(4):e3000046.
- Mathew DJ, Sánchez JM, Passaro C, Charpigny G, Behura SK, Spencer TE, Lonergan P. Interferon tau-dependent and independent effects of the bovine conceptus on the endometrial transcriptome†. Biol Reprod 2019 Feb 1;100(2):365-380.
- Talukder AK, Rashid MB, Yousef MS, Kusama K, Shimizu T, Shimada M, Suarez SS, Imakawa K, Miyamoto A. Oviduct epithelium induces interferon-tau in bovine Day-4 embryos, which generates an anti-inflammatory response in immune cells. Sci Rep 2018 May 18;8(1):7850.
- Lesage-Padilla A, Forde N, Poirée M, Healey GD, Giraud-Delville C, Reinaud P, Eozenou C, Vitorino Carvalho A, Galio L, Raliou M, Oudin JF, Richard C, Sheldon IM, Charpigny G, Lonergan P, Sandra O. Maternal metabolism affects endometrial expression of oxidative stress and FOXL2 genes in cattle. PLoS One 2017;12(12):e0189942.
- Denis M, Dembélé D, Richard C, Leduc M, Pez M, Reinaud P, Dubois O, Kiefer H, Jammes H, Gelin V, Constant F, Vialard F, Foucras G, Germon P, Charpigny G, Sandra O, Raliou M. Ageing-driven molecular and functional changes in the bovine endometrium. PLoS One 2025;20(9):e0332176.
- Wang PC, Liu ZK, Li JR, Zhao ZH, Chang QW, Guo XM, Jin L, Hu YT, Yang Z. Tryptophan regulates the expression of IGFBP1 in bovine endometrial epithelial cells in vitro via the TDO2-AHR pathway. BMC Vet Res 2024 Sep 4;20(1):390.
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